Calcareous spherules produced by intracellular symbiotic bacteria protect the sponge Hemimycale columella from predation better than secondary metabolites

Abstract

Benthic sessile organisms in general, and sponges in particular, have developed an array of defense mechanisms to survive in crowded, resource and/or space-limited environments. Indeed, various defense mechanisms may converge in sponges to accomplish a defensive function in an additive or synergetic way, or to operate at different times during the sponge's life cycle. Moreover, sponges harbor highly diverse microbial communities that contribute in several ways to the host's success. Although some symbiotic bacteria produce chemical compounds that protect the sponge from predation, the possible deterrent function exerted by the calcareous coat of a sponge's endosymbiotic bacterium has not, to date, been explored. Hemimycale columella is an Atlanto-Mediterranean sponge, which produces bioactive metabolites and has been reported to host an intracellular bacterium with a calcite envelope. Calcibacteria accumulate in high densities at the sponge periphery, forming a kind of sub-ectosomal cortex. They have been suggested to provide the sponge with several benefits, one of which is protection from predators. In this study, we assess the relative contribution of the endosymbiotic calcibacteria and bioactive compounds produced by H. columella to defend the sponge against sympatric predators. Deterrence experiments have revealed that the sponge combines >1 defense mechanism to dissuade a large array of potential predators; this represents an example of the evolutionary fixation of redundant mechanisms of defense. The chemicals deterred Paracentrotus lividus, Chromis chromis, Oblada melanura, and Diplodus vulgaris, but not Parablennius incognitus and Coris julis, while the spherules of the symbiotic calcibacteria significantly deterred all predators assayed.

Endosymbiotic calcifying bacteria across sponge species and oceans

“…Conversely, it is generally accepted that for mutualistic symbioses to become evolutionaryly fixed, benefits at the species level should compensate for the costs to the associated partners 41 . The most obvious benefit to sponges from their association with calcifying bacteria is the ‘low cost’ construction of an exoskeleton, which may serve as structural purpose and deter potential sponge predators better than secondary metabolites 42 . Protection against an increase in predators has been proposed as an evolutionary driver of exoskeletons in ancient animals during the Cambrian explosion 43 .…”

“…Siliceous spicules were precipitated and then the pellet was discarded. The spicule-free homogenates were subjected to a series of centrifugations and re-suspensions 42 . One aliquot of the each final spherule suspensions (three per individual) was filtered through 0.2 μm pore filters and filters were CARD-FISH treated ( Table 1 ).…”

Host genetics and geography influence microbiome composition in the spongeIrcinia campana

“…Sponges (phylum Porifera) are considered valuable model systems in host-microbiome research due to the abundance and diversity within their associated microbial communities (Pita, Fraune, & Hentschel, 2016), with a total of 52 bacterial phyla and candidate phyla discovered among sponge hosts (Thomas et al, 2016). Spongemicrobiome interactions are numerous and complex, and microbial symbionts may confer a number of benefits to their host including nutrition and waste metabolism (Freeman, Thacker, Baker, & Fogel, 2013;Karimi et al, 2018;Moitinho-Silva et al, 2017;Thomas, Rusch, et al, 2010), acclimation to ocean acidification (Ribes et al, 2016), reduction in host surface fouling (On, Lau, & Qian, 2006) and production of compounds that deter predation of the sponge host (Garate, Blanquer, & Uriz, 2015). Sponge-associated microbes are also of significant biotechnological interest due to their potential for production of novel, pharmaceutically active secondary metabolites .…”

Sponges and Their Microbiomes Show Similar Community Metrics Across Impacted and Well-Preserved Reefs

“…Indeed, unbalancing of their microbial symbioses has been considered to trigger extensive mass mortalities of sponges in the Mediterranean (Webster et al, 2008; Cebrian et al, 2011), and Red Sea (Gao et al, 2014). In addition, some purported benefits that sponges may obtain from their associations with microbes have also been proposed such as, antifungal activity, production of bioactive compounds against predation, roles in nitrogen and carbon cycle and vitamin biosynthesis (Schmidt et al, 2000; Freeman and Thacker, 2011; Hentschel et al, 2012; Freeman et al, 2013), but rarely have been experimentally demonstrated (de Voogd et al, 2015; Garate et al, 2015).…”